Tobacco smoke: A critical etiological factor for vascular impairment at the blood-brain barrier

Brain Research

Volumn 1287, Issue , 2009, Pages 192-205

  Hossain, M ^a   Sathe, T ^a   Fazio, V ^a   Mazzone, P ^a   Weksler, Babette ^b,c   Janigro, D ^a   Rapp, E ^d   Cucullo, L ^a  

^a CLEVELAND CLINIC LERNER COLLEGE OF MEDICINE   (United States)

^b INSERM   (France)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d Flocel Inc   (United States)

Author keywords

Atherosclerosis; Cerebral blood flow; In vitro; Inflammation; Ischemia; Public health; Shear stress; Smoking; Systemic; Tobacco

Indexed keywords

MATRIX METALLOPROTEINASE; TOBACCO SMOKE;

ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL INJURY; BRAIN BLOOD FLOW; CELL DIFFERENTIATION; CONTROLLED STUDY; HEMODYNAMICS; HUMAN; HUMAN CELL; ISCHEMIA; MACROPHAGE; MICROVASCULATURE; MONOCYTE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; UPREGULATION;

BLOOD-BRAIN BARRIER; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; HUMANS; MICROVESSELS; TOBACCO SMOKE POLLUTION; VASCULAR DISEASES;

NICOTIANA TABACUM;

EID: 68049110323     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.06.033     Document Type: Article

References (62)

1. Abboud S., Viiri L.E., Lutjohann D., Goebeler S., Luoto T., Friedrichs S., Desfontaines P., Gazagnes M.D., Laloux P., Peeters A., Seeldrayers P., Lehtimaki T., Karhunen P., Pandolfo M., and Laaksonen R. Associations of apolipoprotein E gene with ischemic stroke and intracranial atherosclerosis. Eur. J. Hum. Genet. 16 (2008) 955-960
2. Abbruscato T.J., Lopez S.P., Mark K.S., Hawkins B.T., and Davis T.P. Nicotine and cotinine modulate cerebral microvascular permeability and protein expression of ZO-1 through nicotinic acetylcholine receptors expressed on brain endothelial cells. J. Pharm. Sci. 91 (2002) 2525-2538
3. Abbruscato T.J., Lopez S.P., Roder K., and Paulson J.R. Regulation of blood-brain barrier Na,K,2Cl-cotransporter through phosphorylation during in vitro stroke conditions and nicotine exposure. J. Pharmacol. Exp. Ther. 310 (2004) 459-468
4. Almeida O.P., Garrido G.J., Lautenschlager N.T., Hulse G.K., Jamrozik K., and Flicker L. Smoking is associated with reduced cortical regional gray matter density in brain regions associated with incipient Alzheimer disease. Am. J. Geriatr. Psychiatry 16 (2008) 92-98
5. Argacha J.F., Adamopoulos D., Gujic M., Fontaine D., Amyai N., Berkenboom G., and van de B.P. Acute effects of passive smoking on peripheral vascular function. Hypertension 51 (2008) 1506-1511
6. Badolato R., Wang J.M., Murphy W.J., Lloyd A.R., Michiel D.F., Bausserman L.L., Kelvin D.J., and Oppenheim J.J. Serum amyloid A is a chemoattractant: induction of migration, adhesion, and tissue infiltration of monocytes and polymorphonuclear leukocytes. J. Exp. Med. 180 (1994) 203-209
7. Bresgen N., Jaksch H., Bauer H.C., Eckl P., Krizbai I., and Tempfer H. Astrocytes are more resistant than cerebral endothelial cells toward geno- and cytotoxicity mediated by short-term oxidative stress. J. Neurosci. Res. 84 (2006) 1821-1828
8. Butler G.S., Apte S.S., Willenbrock F., and Murphy G. Human tissue inhibitor of metalloproteinases 3 interacts with both the N- and C-terminal domains of gelatinases A and B. Regulation by polyanions. J. Biol. Chem. 274 (1999) 10846-10851
9. Candelario-Jalil E., Yang Y., and Rosenberg G.A. Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience 158 (2009) 983-994
10. Chen M., Li Y., Yang T., Wang Y., Bai Y., and Xie X. ADMA induces monocyte adhesion via activation of chemokine receptors in cultured THP-1 cells. Cytokine 43 (2008) 149-159
11. Chen S.H., Murphy D.A., Lassoued W., Thurston G., Feldman M.D., and Lee W.M. Activated STAT3 is a mediator and biomarker of VEGF endothelial activation. Cancer Biol. Ther. 7 (2008) 1994-2003
12. Chen Z., and Han Z.C. STAT3: a critical transcription activator in angiogenesis. Med. Res. Rev. 28 (2008) 185-200
13. Cicha I., Goppelt-Struebe M., Yilmaz A., Daniel W.G., and Garlichs C.D. Endothelial dysfunction and monocyte recruitment in cells exposed to non-uniform shear stress. Clin. Hemorheol. Microcirc. 39 (2008) 113-119
14. Cucullo L., McAllister M., Kight K., Krizanac-Bengez L., Marroni M., Mayberg M., Stanness K., and Janigro D. A new dynamic in vitro model for the multidimensional study of astrocyte-endothelial cell interactions at the blood-brain barrier. Brain Res. 951 (2002) 243
15. Cucullo L., Aumayr B., Rapp E., and Janigro D. Drug delivery and in vitro models of the blood-brain barrier. Curr. Opin. Drug Discov. Devel. 8 (2005) 89-99
16. Cucullo, L., Hossain, M., Rapp, E., Manders, T., Janigro, D., (2006) Development of a humanized in vitro blood-brain barrier model to screen for brain penetration of antiepileptic drugs, Epilepsia.
17. Cucullo L., Couraud P.O., Weksler B., Romero A., Hossain M., Rapp E., and Janigro D. Immortalized human brain endothelial cells and flow-based vascular modeling: a marriage of convenience for rational neurovascular studies. J. Cereb. Blood Flow Metab 28 (2008) 312-328
18. DiNapoli A., Huber J.D., Houser K., Li X., and Rosen C.L. Early disruptions of the blood-brain barrier may contribute to exacerbated neuronal damage and prolonged functional recovery following stroke in aged rats. Neurobiol. Aging 29 (2008) 753-764
19. Ding G., Jiang Q., Li L., Zhang L., Gang Z.Z., Ledbetter K.A., Ewing J.R., Li Q., and Chopp M. Detection of BBB disruption and hemorrhage by Gd-DTPA enhanced MRI after embolic stroke in rat. Brain Res. 1114 (2006) 195-203
20. Eo H.S., and Kim D.I. Apolipoprotein C1 and apolipoprotein E are differentially expressed in atheroma of the carotid and femoral artery. J. Surg. Res. 144 (2008) 132-137
21. Fan L.J., and Karino T. Effect of serum concentration on adhesion of monocytic THP-1 cells onto cultured EC monolayer and EC-SMC co-culture. J. Zhejiang. Univ Sci. B 9 (2008) 623-629
22. German A.K., and Logiiko V.L. The cerebral blood flow in smokers. Lik. Sprava. (1995) 123-125
23. Gidday J.M., Gasche Y.G., Copin J.C., Shah A.R., Perez R.S., Shapiro S.D., Chan P.H., and Park T.S. Leukocyte-derived matrix metalloproteinase-9 mediates blood-brain barrier breakdown and is proinflammatory after transient focal cerebral ischemia. Am. J. Physiol Heart Circ. Physiol 289 (2005) H558-H568
24. Gill J.S., Shipley M.J., Tsementzis S.A., Hornby R., Gill S.K., Hitchcock E.R., and Beevers D.G. Cigarette smoking. A risk factor for hemorrhagic and nonhemorrhagic stroke, Arch. Intern. Med. 149 (1989) 2053-2057
25. Gloor S.M., Wachtel M., Bolliger M.F., Ishihara H., Landmann R., and Frei K. Molecular and cellular permeability control at the blood-brain barrier. Brain Res. Brain Res. Rev. 36 (2001) 258-264
26. Hawkes C.H. Smoking is a risk factor for multiple sclerosis: a metanalysis. Mult. Scler. 13 (2007) 610-615
27. Horn F., Henze C., and Heidrich K. Interleukin-6 signal transduction and lymphocyte function. Immunobiology 202 (2000) 151-167
28. Howard G., Wagenknecht L.E., Cai J., Cooper L., Kraut M.A., and Toole J.F. Cigarette smoking and other risk factors for silent cerebral infarction in the general population. Stroke 29 (1998) 913-917
29. Huang Z.G., Xue D., Preston E., Karbalai H., and Buchan A.M. Biphasic opening of the blood-brain barrier following transient focal ischemia: effects of hypothermia. Can. J. Neurol. Sci. 26 (1999) 298-304
30. Hutamekalin P., Farkas A.E., Orbok A., Wilhelm I., Nagyoszi P., Veszelka S., Deli M.A., Buzas K., Hunyadi-Gulyas E., Medzihradszky K.F., Meksuriyen D., and Krizbai I.A. Effect of nicotine and polyaromatic hydrocarbons on cerebral endothelial cells. Cell Biol. Int. 32 (2008) 198-209
31. Kaplanski G., Marin V., Fabrigoule M., Boulay V., Benoliel A.M., Bongrand P., Kaplanski S., and Farnarier C. Thrombin-activated human endothelial cells support monocyte adhesion in vitro following expression of intercellular adhesion molecule-1 (ICAM-1; CD54) and vascular cell adhesion molecule-1 (VCAM-1; CD106). Blood 92 (1998) 1259-1267
32. Kelly M.A., Shuaib A., and Todd K.G. Matrix metalloproteinase activation and blood-brain barrier breakdown following thrombolysis. Exp. Neurol. 200 (2006) 38-49
33. Koskinen L.O., Collin O., and Bergh A. Cigarette smoke and hypoxia induce acute changes in the testicular and cerebral microcirculation. Ups. J. Med. Sci. 105 (2000) 215-226
34. Koto T., Takubo K., Ishida S., Shinoda H., Inoue M., Tsubota K., Okada Y., and Ikeda E. Hypoxia disrupts the barrier function of neural blood vessels through changes in the expression of claudin-5 in endothelial cells. Am. J. Pathol. 170 (2007) 1389-1397
35. Krizanac-Bengez L., Mayberg M.R., Cunningham E., Hossain M., Ponnampalam S., Parkinson F.E., and Janigro D. Loss of shear stress induces leukocyte-mediated cytokine release and blood-brain barrier failure in dynamic in vitro blood-brain barrier model. J. Cell Physiol 206 (2006) 68-77
36. Mannami T., Iso H., Baba S., Sasaki S., Okada K., Konishi M., and Tsugane S. Cigarette smoking and risk of stroke and its subtypes among middle-aged Japanese men and women: the JPHC Study Cohort I. Stroke 35 (2004) 1248-1253
37. Marchi N., Angelov L., Masaryk T., Fazio V., Granata T., Hernandez N., Hallene K., Diglaw T., Franic L., Najm I., and Janigro D. Seizure-promoting effect of blood-brain barrier disruption. Epilepsia 48 (2007) 732-742
38. Mast H., Thompson J.L., Lin I.F., Hofmeister C., Hartmann A., Marx P., Mohr J.P., and Sacco R.L. Cigarette smoking as a determinant of high-grade carotid artery stenosis in Hispanic, black, and white patients with stroke or transient ischemic attack. Stroke 29 (1998) 908-912
39. McMullen C.B., Fleming E., Clarke G., and Armstrong M.A. The role of reactive oxygen intermediates in the regulation of cytokine-induced ICAM-1 surface expression on endothelial cells. Mol. Cell Biol. Res. Commun. 3 (2000) 231-237
40. Meyer J.S., Rauch G., Rauch R.A., and Haque A. Risk factors for cerebral hypoperfusion, mild cognitive impairment, and dementia. Neurobiol. Aging 21 (2000) 161-169
41. Meyer J., Tauh J., and Galla H.G. The susceptibility of cerebral endothelial cells to astroglial induction of blood-brain barrier enzymes depends on their proliferative state. J Neurochem. 57 (1991) 1971-1977
42. Miller G.J., Bauer K.A., Cooper J.A., and Rosenberg R.D. Activation of the coagulant pathway in cigarette smokers. Thromb. Haemost. 79 (1998) 549-553
43. Minagar A., and Alexander J.S. Blood-brain barrier disruption in multiple sclerosis. Mult. Scler. 9 (2003) 540-549
44. Nordskog B.K., Blixt A.D., Morgan W.T., Fields W.R., and Hellmann G.M. Matrix-degrading and pro-inflammatory changes in human vascular endothelial cells exposed to cigarette smoke condensate. Cardiovasc. Toxicol. 3 (2003) 101-117
45. Nordskog B.K., Fields W.R., and Hellmann G.M. Kinetic analysis of cytokine response to cigarette smoke condensate by human endothelial and monocytic cells. Toxicology 212 (2005) 87-97
46. Ohtsuki S., Sato S., Yamaguchi H., Kamoi M., Asashima T., and Terasaki T. Exogenous expression of claudin-5 induces barrier properties in cultured rat brain capillary endothelial cells. J. Cell Physiol 210 (2007) 81-86
47. Rahman M.M., and Laher I. Structural and functional alteration of blood vessels caused by cigarette smoking: an overview of molecular mechanisms. Curr. Vasc. Pharmacol. 5 (2007) 276-292
48. Romanic A.M., White R.F., Arleth A.J., Ohlstein E.H., and Barone F.C. Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 29 (1998) 1020-1030
49. Rosenberg G.A., and Yang Y. Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia. Neurosurg. Focus. 22 (2007) E4
50. Santaguida S., Janigro D., Hossain M., Oby E., Rapp E., and Cucullo L. Side by side comparison between dynamic versus static models of blood-brain barrier in vitro: A permeability study. Brain Res. 1109 (2006) 1-13
51. Schroder R., and Linke R.P. Cerebrovascular involvement in systemic AA and AL amyloidosis: a clear haematogenic pattern. Virchows Arch. 434 (1999) 551-560
52. Sellebjerg F., and Sorensen T.L. Chemokines and matrix metalloproteinase-9 in leukocyte recruitment to the central nervous system. Brain Res. Bull. 61 (2003) 347-355
53. Shen Y., Rattan V., Sultana C., and Kalra V.K. Cigarette smoke condensate-induced adhesion molecule expression and transendothelial migration of monocytes. Am. J. Physiol 270 (1996) H1624-H1633
54. Shigemori Y., Katayama Y., Mori T., Maeda T., and Kawamata T. Matrix metalloproteinase-9 is associated with blood-brain barrier opening and brain edema formation after cortical contusion in rats. Acta Neurochir. Suppl 96 (2006) 130-133
55. Shinton R., and Beevers G. Meta-analysis of relation between cigarette smoking and stroke. BMJ 298 (1989) 789-794
56. Sundstrom P., Nystrom L., and Hallmans G. Smoke exposure increases the risk for multiple sclerosis. Eur. J. Neurol. 15 (2008) 579-583
57. Svedin P., Hagberg H., Savman K., Zhu C., and Mallard C. Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia-ischemia. J. Neurosci. 27 (2007) 1511-1518
58. Torikai K., Uwano Y., Nakamori T., Tarora W., and Takahashi H. Study on tobacco components involved in the pyrolytic generation of selected smoke constituents. Food Chem. Toxicol. 43 (2005) 559-568
59. Wang L., Kittaka M., Sun N., Schreiber S.S., and Zlokovic B.V. Chronic nicotine treatment enhances focal ischemic brain injury and depletes free pool of brain microvascular tissue plasminogen activator in rats. J. Cereb. Blood Flow Metab 17 (1997) 136-146
60. Wong D., Dorovini-Zis K., and Vincent S.R. Cytokines, nitric oxide, and cGMP modulate the permeability of an in vitro model of the human blood-brain barrier. Exp. Neurol. 190 (2004) 446-455
61. Xu Y., Yamada T., Satoh T., and Okuda Y. Measurement of serum amyloid A1 (SAA1), a major isotype of acute phase SAA. Clin. Chem. Lab Med. 44 (2006) 59-63
62. Zhang J., Liu Y., Shi J., Larson D.F., and Watson R.R. Side-stream cigarette smoke induces dose-response in systemic inflammatory cytokine production and oxidative stress. Exp. Biol. Med. (Maywood.) 227 (2002) 823-829